Научная статья на тему 'Fungi of the Russian Far East. 3. Species of Amanita (Basidiomycota) new to Russia from the Primorye Territory'

Fungi of the Russian Far East. 3. Species of Amanita (Basidiomycota) new to Russia from the Primorye Territory Текст научной статьи по специальности «Биологические науки»

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Ключевые слова
AMANITA / ДАЛЬНИЙ ВОСТОК РОССИИ / RUSSIAN FAR EAST / НОВЫЕ НАХОДКИ / NEW RECORDS / МОРФОЛОГИЯ / MORPHOLOGY / ITS

Аннотация научной статьи по биологическим наукам, автор научной работы — Malysheva E.F., Kiyashko A.A., Kovalenko A.E.

Amanita pallidorosea, A. longistriata and A. farinosa are recorded for the first time for Russia from the Primorye Territory. Their descriptions and illustrations are provided.

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Грибы Дальнего Востока России. 3. Новые для России виды рода Amanita (Basidiomycota) из Приморского края

В статье приводятся подробные описания и иллюстрации трех новых для России видов рода Amanita (A. pallidorosea, A. longistriata и A. farinosa), найденных в Приморском крае.

Текст научной работы на тему «Fungi of the Russian Far East. 3. Species of Amanita (Basidiomycota) new to Russia from the Primorye Territory»

Fungi of the Russian Far East. 3. Species of Amanita

(Basidiomycota) new to Russia from the Primorye Territory

E. F. Malysheva, A. A. Kiyashko, A. E. Kovalenko

Komarov Botanical Institute, Prof. Popov Str., 2, St. Petersburg, 197376, Russia; [email protected]

Abstract. Amanita pallidorosea, A. longistriata and A. farinosa are recorded for the first time for Russia from the Primorye Territory. Their descriptions and illustrations are provided.

Keywords: Amanita, Russian Far East, new records, morphology, ITS.

Грибы Дальнего Востока России. 3. Новые для России виды рода Amanita (Basidiomycota) из Приморского края

Е. Ф. Малышева, А. А. Кияшко, А. Е. Коваленко

Ботанический институт им. В. Л. Комарова РАН, ул. Профессора Попова, д. 2, Санкт-Петербург, 197376, Россия; [email protected]

Резюме. В статье приводятся подробные описания и иллюстрации трех новых для России видов рода Amanita (A. pallidorosea, A. longistriata и A. farinosa), найденных в Приморском крае.

Ключевые слова: Amanita, Дальний Восток России, новые находки, морфология, ITS.

The genus Amanita Pers. is one of the well-known genera in Basidiomycota distributed worldwide. Most species are known to be ectomycor-rhizal with different forest trees and play an important role in ecosystems. More than 500 species are described in the world (Yang, 2000). During the past decade, the genus Amanita has received much taxonomical attention in temperate and tropical regions and more than 10 new taxa have been described (Yang et al., 2001, 2004; Zhang et al., 2010). However, the knowledge about the genus from the Primorye Territory is rather limited — no more than sixteen Amanita species were registered at present (Vassilieva, 1973; Flora..., 2006, 2007). Our intensive investigation on agaricoid fungi demonstrated that the diversity of Amanita is much higher in the Primorye Territory than previously reported in mentioned papers. This paper is a part of a series dealing with the agaricoid fungi of the Russian Far East (Malysheva et al., 2013; Kiyashko et al, 2014).

Materials and Methods

Studied specimens were collected in 2011-2013. Macromorphological descriptions were based on the fresh material and colour photos of basidi-

ocarps. Colour codes are given based on A. Kornerup and J. H. Wanscher (1978). Micromorphological data were obtained from the dried material mounted in 5 % KOH, Congo Red or Melzer's reagents using AxioImag-erA1 light microscope and a Zeiss AxioCam MRc5 digital camera with AxioVision SE64 version 4.8.3.0 software. In basidiospore dimensions Q is used to mean «length/width ratio» of a spore in side view; Q means the average Q of all spores measured ± standard deviation. The total number of basidiospores measured for each taxon was not less than thirty. The drawings were performed with Inkscape version 0.48 free software.

Collected specimens were deposited in the Mycological Herbarium of the Komarov Botanical Institute RAS (LE). All sequences newly generated for this study were deposited in GenBank with corresponding accession numbers.

Results

As a result of studying Amanita species collected during the mycolo-gical expeditions to the Sikhote-Alin and Kedrovaya Pad' Nature Reserves, three noteworthy and new to Russia species were discovered. All these species are described and illustrated herein.

Amanita farinosa Schwein., 1822, Schriften Naturf. Ges. Leipzig, 1: 79 (Fig. 1; Plate I, 3).

B as idi ocarps small-sized. P ileus 20 mm in diam., hemispherical when young, then convex, becoming plano-convex with slightly depressed centre, dry, with powder-like volval remnants all over the surface but more dense in the centre; birch bark or brownish grey (6B2, 6C2) or sepia, with pale ochre margin; margin strongly tuberculate-striate up to half the radius, non-appendiculate. Lamellae almost free, just touching stipe, subcrowded, white, with concolourous and slightly flocculose edge; lamellulae truncate. Stipe 30 x 3.5 mm, subcylindric, slightly broadened towards base, without distinct basal bulb; whitish to pale yellow or yellowish white (3A2), entirely flocculose, having distinct brownish powdery area of universal veil at base. A nnulu s absent.

Lamellar trama bilateral. Subhymenium 25-40 ^m thick, with several layers of globose, subglobose or broadly clavate, hyaline and thin-walled cells, 12-20 x 8-16 ^m. Basidia 27-36 x 7-10 ^m, clavate, 4-spored, without basal clamps. Basidiospores 7.8-9.2(9.5) x (5.6) 6-7(7.6) ^m [Q = (1.11)1.18-1.47(1.53), Q = 1.31 ± 0.11], broadly ellipsoid to ellipsoid, rarely elongate, inamyloid, thin-walled, hyaline; apiculus small, sublateral. Lamellar edge sterile, composed of numerous subglobose, clavate or ovoid elements, 8-23 x 6-13.5 pm, single

Fig. 1. Microscopic features of Amanita farinosa (LE 296435). a — basidiospores; b — cells of lamellar edge; c — basidia and elements of subhymenium; d — elements of powdery volva at stipe base. Scale bar: 10 p,m.

or in short chains, hyaline, thin-walled. P ileipellis 90-180 ^m thick; the upper layer comprising, interwoven and slightly branched, densely arranged, filamentous hyphae 2-4 ^m wide, thin- or slightly thick-walled, hyaline or yellowish brown; the lower layer has similar structure, hyphae up to 6 ^m wide. Volval remnants on pileus surface made up of scattered, interwoven and anastomosing, sometimes inflated, filamentous hyphae, 2.7-8 ^m wide, slightly thick-walled, hyaline; mixed with numerous, strongly inflated, subglobose, ellipsoid, oviform or pyriform,

thick-walled cells, 15-60 x 15-50 цш, with brown intracellular pigment. Powdery volva at stipe base consisting of anastomosing filamentous, slightly thick-walled hyphae, 5-11 цш wide, often with inflated single segments, hyaline or yellowish, occasionally incrusted; mixed with plentiful subglobose, pyriform, subcylindrical or ellipsoid elements, 15-55 x 8-45 цш, often in short chains, thick-walled, with pale yellow-brown intracellular pigment. Clamps absent in all tissues.

Habitat and distribution: Solitary on soil in mixed forest. Distributed in eastern USA, southeastern Canada and Costa Rica. Recently it has been found in eastern Asia (Kim et al, 2013b).

Specimen examined: Russia, Primorye Territory, Kedrova-ya Pad' Nature Reserve, valley of Kedrovaya River, coniferous-broad-leaved forest, on soil, 08.09.2011, A. Kovalenko, LE 296435, GenBank KJ739808 (ITS), KJ739815 (LSU).

Note: Amanita farinosa belongs to the subgenus Amanita section Amanita (Tu-loss, 2014c). This species is similar to several taxa which also have pulverulent pileus surface and small- to medium-sized basidiocarps: A. obsita Corner et Bas, A. nehuta J. S. Ridl. and A. subvaginata (Cleland et Cheel) E.-J. Gilbert. A. obsita differs from A. farinosa by light-coloured pileus and smaller basidiospores [(5.5)6.5-7 x 5.5-6.5(7) цш] (Sanmee et al, 2008). A. nehuta, originally described from New Zealand, has larger and robust basidiocarps with distinct basal bulb on stipe and appendiculate pileus margin (Tulloss, 2014a). A. subvaginata, known from Australia, can be separated from A. farinosa by its pileus coloration, bulbose base with marginate volva and globose basidiospores (Tulloss, 2014b).

Amanita longistriata S. Imai, 1938, J. Coll. agric., Hokkaido Imp. Univ. 43: 11. (Fig. 2; Plate I, 1, 2).

Basidiocarps medium- to large-sized. Pileus 60-80 mm in diam., hemispherical when young, then convex, becoming applanate, with low broad umbo or with depressed centre, glabrous, often viscid or sub-viscid when wet, with volval remnants in the form of appressed to innate small patches or squamules, concolorous with surface, densely arranged at centre and scarce towards margin; greyish brown, light brown (6D3-4) or brown (6E4) with pale margin, sometimes very light-coloured, with almost white or pinkish (7A2-3) margin and darker disc; margin strongly striate or sulcate up to half the radius, often undulating, non-appendicu-late. Lamellae free, just touching stipe or almost narrowly adnate, subdistant, pinkish white then pink, with flocculose to subdenticulate, whitish or concolourous edge; lamellulae not defined. Stipe 90-150 x 8-15 mm, subcylindric, slightly broadened towards base, hollow, without distinct basal bulb; whitish to yellowish or pinkish white (3A2, 7A2), flocculose-squamulose above annulus, smooth below. Volva caliciform or saccate, thin and membranous, sometimes rather thick, firm, with free

Fig. 2. Microscopic features of Amanita longistriata (LE 296426). a — basidiospores; b — basidia and elements of subhymenium; c — cells of lamellar

edge. Scale bar: 10 p.m.

wide limb, often lobed, outer surface velvety, both surface white. Annul u s present, at upper part of stipe, rather wide, thin, membranous, fragile, white, with floccose edge and striate outer surface.

Lamellar trama bilateral. Subhymenium 27-40 ^m thick, with 2-3 layers of globose, subglobose, broadly clavate or irregularly shaped, hyaline and thin-walled cells, 10-20 x 7-18 ^m. Basidia 40-70(80) x 8-16 ^m, clavate, 4-spored, with basal clamps.

Basidiospores 10-13(16) x (7.8)8.2-10.5(11.6) ^m [Q = (1.03)1.15-1.36(1.47), Q = 1.26 ± 0.06], broadly ellipsoid or ellipsoid, rarely sub-globose, inamyloid, thin-walled, hyaline; apiculus small, sublateral. Lamellar edge sterile, composed of numerous subglobose, clavate or pyriform cells, 20-60 x 15-45 p,m, single or in short chains, hyaline, thin-walled. Pileipellis 90-120 ^m thick; the upper layer up to 60 p,m, gelatinized, comprising filamentous, undifferentiated, hyaline hyphae 8-11 ^m wide; the lower layer (30-60 ^m thick) made up of more compactly arranged, interwoven, filamentous, thin-walled, hyaline or with intracellular yellowish pigment hyphae 7-10 ^m wide. Volval limb on the stipe base made up of interwoven, thin-walled, hyaline, sometimes anastomosing, filamentous hyphae 3-12 ^m wide; terminal elements numerous, strongly inflated, ellipsoid, clavate, oviform or subglobose, thin-walled, 40-100 x 20-55 ^m; vascular hyphae rare, tortuous, up to 7 ^m wide; inner surface of the limb gelatinized, comprises interwoven, filamentous thin-walled hyphae 2-4.5 ^m wide; outer surface of the limb consisting of interwoven, filamentous, thin-walled hyphae 2.5-6 ^m wide, hyaline or with yellow-brown intracellular pigment; inflated cells rare. Annulus consisting of branching and anastomosing, interwoven, thin- or slightly thick-walled, 2.5-7 ^m wide filamentous hyphae, mixed with occasional, hyaline, thin-walled, subglobose, broadly ellipsoid or pyriform terminal cells, 20-40 x 15-30 ^m; vascular hyphae scattered, hyaline, up to 6 ^m wide. Clamps common in all tissues.

Habitat and distribution: Solitary or scattered on soil in mixed or coniferous forests. It was originally described from Japan. Also known from South Korea and China (Yang, Doi, 1999).

Specimens examined: Russia, Primorye Territory, Sikhote-Alin Nature Reserve, vicinity of Yasnaya Reserve station, coniferous-broadleaved forest, on soil, 21.08.1996, A. Kovalenko, LE 296421; ibid., floodplain of Yasnaya River, coniferous-broadleaved forest (Larix, Betula and Quercus), on soil, 27.08.2013, E. Malysheva, LE 296419, GenBank KJ739810 (ITS); ibid., floodplain of Yasnaya River, mixed forest, on soil, 21.08.2013, O. Morozova, LE 296420, GenBank KJ739811 (ITS); the same reserve, vicinity of Ust'-Serebryany reserve station, bank of Sere-bryanka River, oak forest with sporadic birch, maple and coniferous trees, 04.09.1996, O. Morozova, LE 296429, GenBank KJ739812 (ITS); the same reserve, upper stream Sukhoi, mixed forest (Quercus mongolica, Betula costata, Pinus koraiensis), on soil, 44°59'44" N, 136°30'18" E, 10.08.2012, A. Kiyashko, LE 296426, GenBank KJ739809 (ITS).

Note: Amanita longistriata belongs to the subgenus Amanita section Caesareae Singer. The remarkable features of this species are its strongly striate pileus and beau-

tiful clearly pink lamellae. Based on combination of these characters A. longistriata resembles A. incarnatifolia Z. L. Yang in the field. The latter, originally described from pine forests China from, differs from A. longistriata by shorter striation of pileus margin and narrower basidiospores (not exceeding 9 цш broadwise) (Yang, 1997). Another representative of sect. Caesareae having distinctly pink lamellae is A. roseolamellata A. E. Wood, but it differs from A. longistriata at least by conspicuously narrower basidiospores [6-8.5(9) цш wide] and occurring in specific sclerophyll forests in Australia (Wood, 1997).

Amanita pallidorosea P. Zhang et Zhu L. Yang, 2010, Fungal Diversity, 42: 125 (Fig. 3; Plate II).

Basidiocarps medium- to large-sized. Pileus 30-95 mm in diam., hemispherical, ovoid or rounded conical when young, then broadly conical, convex, becoming applanate with low broad umbo, glabrous, often subviscid when wet, with yellowish white umbo (4A3-4) surrounded by pinkish (9A2-3, 10A2-3) or pastel red (9A4) circle, becoming white to whitish toward margin; margin slightly incurved, faintly striate or non-striate, non-appendiculate. Lamellae free, crowded, white or slightly pinkish with age, with concolorous edges. Stipe 90-160 x 6-13 mm, subcylindric, slightly broadened towards base, with distinct basal bulb up to 3 cm wide; whitish to yellowish white (3A2-3), covered with white flaked squamules in numerous belts. Vo l v a membranous, firm, with free wide limb, outer surface velvety, both surface white. Annulus present, at upper part of stipe, wide, thin, membranous, rather stable, with undulating edge, white or slightly yellowish.

Lamellar trama bilateral. Subhymenium 18-35 цш thick, with 2-4 layers of globose, subglobose, broadly clavate or irregularly shaped, hyaline and thin-walled cells, 8-22 x 7-15 цш. Basidia 2740 x 8-11 цш, clavate, 4-spored. Basidiospores 6.8-8.2(9.5) x 6.8-7.8(9) цш [Q = 1.05-1.05(1.1), Q = 1.02 ± 0.03], globose to sub-globose, amyloid, thin-walled, hyaline; apiculus small, sublateral. Lamellar edge sterile, composed of numerous subglobose, clavate or broadly utriform cells, 19-50 x 8-25 цш, single or in short chains, hyaline, thin-walled. Pileipellis 100-150 цш thick; the upper layer up to 100 цш, slightly gelatinized, comprising filamentous undifferentiated, hyaline hyphae 8-12 цш wide; the lower layer (50-60 цш thick) made up of more compactly arranged, interwoven, non-gelatinized, filamentous, thin-walled, hyaline or with intracellular yellowish pigment hyphae 8-10 цш wide. Volval limb at the stipe base made up of loosely interwoven, thin-walled, hyaline, sometimes anastomosing, filamentous hy-phae 4-10 цш wide; terminal elements strongly inflated, subcylindrical, clavate, oviform or subglobose, thin-walled, 40-65 x 12-27 цш; inner surface of the limb gelatinized, comprises filamentous thin-walled

Fig. 3. Microscopic features of Amanitapallidorosea (LE 296427). a — basidiospores; b — cells of lamellar edge; c — basidia and elements of subhymenium. Scale bar: 10 p,m.

hyphae 2.7-5.5 ^m wide; outer surface of the limb comprises filamentous thin-walled hyphae up to 10 ^m wide. Annulus composed of branching and anastomosing, interwoven, thin- or slightly thick-walled, 3-8 ^m wide filamentous hyphae, mixed with numerous, hyaline, slightly thick-walled, globose, broadly ellipsoid or pyriform terminal cells, 25100 x 20-50 ^m. Cl amp s absent in all tissues.

Habitat and distribution: Solitary or scattered on soil in forests with Quercus mongolica. Originally described from China. Also known from Korea (Kim et al, 2013a). Presently known that Amanita pallidorosea is ectomycorrhizal fungus of Fagaceae.

Specimens examined: Russia, Primorye Territory, Sikhote-Alin Nature Reserve, Baklanya mountain, dry oak forest with Quercus mongolica, on soil, 44°54'814" N, 136°32'127" E, 18.08.2013, E. Maly-sheva, LE 296434, GenBank KJ739813 (ITS); ibid., 18.08.2013, E. Maly-sheva, O. Morozova, LE 296427, GenBank KJ739814 (ITS).

Note: Amanita pallidorosea belongs to the subgenus Lepidella (E.-J. Gilbert.) Corner et Bas section Phalloideae (Fr.) Quel. The main distinguishing character of this species is rose tint of its pileus, but entirely white basidiocarps are also typical for this taxon. In the field the latter forms can be mistaken for Amanita virosa (Fr.) Bertill., A. subjunquillea var. alba Z. L. Yang, A. oberwinklerana Z. L. Yang et Y. Doi, A. bisporigera Atk. and A. ocreata Peck on account of the large and whitish basidi-ocarps of similar appearance. A. virosa differs from A. pallidorosea by larger and more ellipsoid basidiospores (8-11 x 7.5-10 цш), longer basidia and different structure of annulus (Neville, Poumarat, 2004). A. subjunquillea var. alba, originally described from China, never has rose tint in pileus, besides its basidiocarp has a distinct yellow reaction with 5 % KOH. A. oberwinklerana, described from Japan, is distinguished from A. pallidorosea by the presence of volval remnants on pileus and larger ellipsoid basidiospores [(7.5)8-10.5(12.5) x (5.5)6.5-8(8.5) цш] (Yang, Doi, 1999). Both A. bisporigera and A. ocreata are known only from North America. A. bisporigera has predominantly 2-spored basidia and slightly larger basidiospores (Tulloss et al., 1995). A. ocreata differs in having larger basidiospores [(6.8) 8.8-12.0(13.8) x (5.9)6.3-8.5(10.8) цш] and yellow reaction with 5 % KOH.

Discussion

Amanita farinosa is found only once in the Primorye Territory in co-niferous-broadleaved forest. The species seems to be rare in the studied area, though its small-sized basidiocarps may be overlooked in the field causing underestimation of its actual occurrence.

Amanita longistriata is common in the Sikhote-Alin Nature Reserve and was collected in different types of forest. It is probably a mycorrhizal symbiont of several taxa of coniferous trees. A. longistriata, recorded in Japan, differs by light-coloured pileus, absence of volval remnants on the pileus surface and shorter basidiospores [(8)9-12(13.5) цш lengthwise], according to description given by some authors (Yang, Doi, 1999); other characters agree with our collections. Nevertheless, the ITS sequences of our collections (LE 296426, LE 296419, LE 296420) are 100 % identical with sequence from Japan (GenBank AB015678).

Amanita pallidorosea is one of the deadly poisonous species from the section Phalloideae. In the Sikhote-Alin Nature Reserve this species was found repeatedly in oak forests where it had abundant fruiting. Noteworthy, that it was recorded simultaneously with other very similar species A. virosa in the same plant communities. Due to difficulties in separating these two species, A. pallidorosea was probably known before in

the studied territory under the name A. virosa. In the Primorye Territory A. pallidorosea is supposed to form ectomycorrhiza with Quercus mongolica. Molecular data showed 100 % identity of the ITS sequences of our specimens of A. pallidorosea (LE 296434, LE 296427) with three Chinese sequences retrieved from GenBank (JX998037, JX998036 and FJ176735) and only four bases differences with sequence of Korean specimen (KF245915), suggesting conspecificity of collections from the different geographical sites.

Acknowledgements

We are very grateful to Dr. E. A. Pimenova and Dr. M. N. Gromyko (Sikhote-Alin Nature Reserve) for the organization of expedition. We thank Dr. O. V. Morozova (Komarov Botanical Institute) who kindly provided some specimens. This study was supported by the Russian Foundation for Basic Research (project № 13-04-00110).

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Литература

[Flora...] Флора, растительность и микобиота заповедника «Уссурийский» / Аз-букина З. М., Бардунов Л. В., Безделева Т. А., Богачева А. В., Буллах Е. М., Васильева Лар. Н., Говорова О. К., Егорова Л. Н., Жабыко Е. В., Никулина Т. В., Родникова И. М., Скирина И. Ф., Таранков В. И., Федина Л. А., Черданце-ва В. Я. 2006. Владивосток: 300 с.

[Flora.] Флора, микобиота и растительность заповедника «Бастак». 2007. Владивосток: 283 с.

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Plate I. Basidiocarps.

1 — Amanita longistriata (LE 296426); 2 — Amanita longistriata (LE 294419); 3 — Amanita farinosa (LE 296435). Scale bars: 1 cm.

Plate II. Basidiocarps of Amanita pallidorosea. 1 — LE 296434; 2 — LE 296427. Scale bars: 1 cm.

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